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A Comparative Analysis of Whole Plastid A Comparative Analysis of Whole Plastid Genomes from the Apiales: Expansion and Contraction of the Inverted Repeat, Mitochondrial to Plastid Transfer of DNA, and Identification of Highly Divergent Noncoding Regions Source: Systematic Botany, 40(1):336-351. Published By: The American Society of Plant Taxonomists URL: http://www.bioone.org/doi/full/10.1600/036364415X686620 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Systematic Botany (2015), 40(1): pp. 336–351 © Copyright 2015 by the American Society of Plant Taxonomists DOI 10.1600/036364415X686620 Date of publication February 12, 2015 A Comparative Analysis of Whole Plastid Genomes from the Apiales: Expansion and Contraction of the Inverted Repeat, Mitochondrial to Plastid Transfer of DNA, and Identification of Highly Divergent Noncoding Regions Stephen R. Downie1,4 and Robert K. Jansen2,3 1Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, U. S. A. 2Department of Integrative Biology, The University of Texas at Austin, Austin, Texas 78712, U. S. A. 3Department of Biological Sciences, Faculty of Science, King Abdulaziz University, P. O. Box 80141, Jeddah 21589, Saudi Arabia 4Author for correspondence ([email protected]) Communicating Editor: Mark P. Simmons Abstract—Previous mapping studies have revealed that the frequency and large size of inverted repeat junction shifts in Apiaceae plastomes are unusual among angiosperms. To further examine plastome structural organization and inverted repeat evolution in the Apiales (Apiaceae + Araliaceae), we have determined the complete plastid genome sequences of five taxa, namely Anthriscus cerefolium (154,719 base pairs), Crithmum maritimum (158,355 base pairs), Hydrocotyle verticillata (153,207 base pairs), Petroselinum crispum (152,890 base pairs), and Tiedemannia filiformis subsp. greenmanii (154,737 base pairs), and compared the results obtained to previously published plastomes of Daucus carota subsp. sativus and Panax schin-seng. We also compared the five Apiaceae plastomes to identify highly variable noncoding loci for future molecular evolutionary and systematic studies at low taxonomic levels. With the exceptions of Crithmum and Petroselinum, which each demonstrate a ~1.5 kilobase shift of its LSC-IRB junction (JLB), all plastomes are typical of most other non-monocot angiosperm plastid DNAs in their structural organization, gene arrangement, and gene content. Crithmum and Petroselinum also incorporate novel DNA in the LSC region adjacent to the LSC-IRA junction (JLA). These insertions (of 1,463 and 345 base pairs, respectively) show no sequence similarity to any other region of their plastid genomes, and BLAST searches of the Petroselinum insert resulted in multiple hits to angiosperm mitochondrial genome sequences, indicative of a mitochondrial to plastid transfer of DNA. A comparison of pairwise sequence divergence values and numbers of variable and parsimony-informative alignment positions (among other sequence characteristics) across all introns and intergenic spacers >150 base pairs in the five Apiaceae plastomes revealed that the rpl32-trnL, trnE-trnT, ndhF-rpl32, 50rps16-trnQ,andtrnT-psbD intergenic spacers are among the most fast-evolving loci, with the trnD-trnY-trnE-trnT combined region presenting the greatest number of potentially informative characters overall. These regions are therefore likely to be the best choices for molecular evolutionary and systematic studies at low taxonomic levels. Repeat analysis revealed direct and inverted dispersed repeats of 30 base pairs or more that may be useful in population-level studies. These structural and sequence analyses contribute to a better understanding of plastid genome evolution in the Apiales and provide valuable new information on the phylogenetic utility of plastid noncoding loci, enabling further molecular evolutionary and phylogenetic studies on this economically, ecologically, and medicinally important group of flowering plants. Keywords—Apiaceae, Araliaceae, intergenic spacer regions, intracellular transfer, plastid DNA. The plastid genomes of the majority of photosynthetic closely related species (Goulding et al. 1996; Plunkett and angiosperms are highly conserved in structural organization, Downie 2000). Large IR expansions (>1,000 bp) occur less gene arrangement, and gene content (Palmer 1991; Raubeson frequently and outnumber large contractions (Plunkett and and Jansen 2005; Wicke et al. 2011; Jansen and Ruhlman 2012; Downie 2000; Raubeson and Jansen 2005; Hansen et al. 2007). Ruhlman and Jansen 2014). Their hallmark is the presence of Because major changes in position of IR junctions can accom- two large duplicate regions in reverse orientation known as pany structural rearrangements elsewhere in the plastid the inverted repeat (IR), which separate the remainder of the genome (Palmer 1991; Boudreau and Turmel 1995; Aii et al. genome into large single copy (LSC) and small single copy 1997; Cosner et al. 1997; Perry et al. 2002; Chumley et al. 2006; (SSC) regions. Variation in size of this molecule is due most Haberle et al. 2008; Guisinger et al. 2011; Wicke et al. 2011), typically to the expansion or contraction of the IR into or out the availability of sequence data for these genomes can help of adjacent single-copy regions and/or changes in sequence elucidate the mechanisms responsible for these large-scale IR complexity due to insertions or deletions of novel sequences. junction shifts and other major genomic changes. Of the two equimolar structural isomers existing for plastid Previous ptDNA restriction site mapping studies have DNA (ptDNA; Palmer 1983), the structure most commonly shown that Apiaceae (Umbelliferae) exhibit unprecedented presented follows the convention used for Nicotiana tabacum variation in position of their LSC/IR boundary regions L. (tobacco) in which one copy of the IR is flanked by genes (Palmer 1985a; Plunkett and Downie 1999, 2000). While most ycf1 and trnH-GUG (and is designated as IRA) and the other umbellifer species surveyed possess a JLB indistinguishable copy is flanked by genes rps19 and ndhF (and is designated as from that of Nicotiana tabacum and the vast majority of other IRB; Shinozaki et al. 1986; Yukawa et al. 2005). The junctions eudicots, at least one expansion and seven different contrac- between the LSC region and each of these IR copies are des- tions of the IR relative to the N. tabacum JLB were detected in ignated as JLA (LSC/IRA) and JLB (LSC/IRB), and the junc- 55 species, each ranging in size from ~1–16 kilobase pairs tions flanking the SSC region are designated as JSA (SSC/IRA) (kb; Plunkett and Downie 2000). As examples, all examined and JSB (SSC/IRB; Shinozaki et al. 1986). In most non-monocot members of the “Aegopodium group,” representatives of angiosperm ptDNAs, JLB lies within the ribosomal protein tribes Careae and Pyramidoptereae (Downie et al. 2010), S10 operon in a more or less fixed position within or near have a ~1.1 kb expansion of JLB relative to that of N. tabacum. the rps19 gene and JLA lies just downstream of LSC gene Careae and Pyramidoptereae are monophyletic sister groups trnH-GUG. The IRs of angiosperm plastomes can fluctuate (Banasiak et al. 2013), indicating that IR junction shifts have greatly in size, although small contractions and expansions the potential to demarcate major clades within the family. of <100 base pairs (bp) are most frequent, and the positions Coriandrum sativum L. and Bifora radians M. Bieb., both of tribe of all four IR/single-copy junctions can vary even among Coriandreae, have the most contracted IRs, approximately 336 2015] DOWNIE AND JANSEN: COMPARISON OF APIALES PLASTID GENOMES 337 16.1 kb smaller than that of N. tabacum. Coriandrum also has a represent tribe Scandiceae subtribes Scandicinae and Daucinae, ~5.7 kb insertion of unknown composition in the vicinity of respectively, Crithmum is classified in tribe Pyramidoptereae, the 16S rRNA gene near the terminus of the IR (Plunkett Tiedemannia represents tribe Oenantheae (Feist et al. 2012), and and Downie 2000), a region subsequently identified through Petroselinum is placed in tribe Apieae (Downie et al. 2010). entire plastome sequencing as a duplication of genes trnH- Crithmum and Petroselinum are members of the “apioid GUG and psbA (Peery et al. 2006). Several of these junction superclade” (Downie et al. 2010), and Hydrocotyle and Panax shifts in Apiaceae are parsimony-informative and all are are classified in the closely related family Araliaceae (Nicolas restricted to the “apioid superclade” of Apiaceae subfamily and Plunkett 2009). To identify the
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